Auditing protein therapeutics management by professional APCs: Toward prevention of immune responses against therapeutic proteins

Journal of Immunology

Volumn 181, Issue 3, 2008, Pages 1609-1615

  Dasgupta, Suryasarathi ^a   Bayry, Jagadeesh ^b   André, Sebastien ^b   Dimitrov, Jordan D ^b   Kaveri, Srinivas V ^b   Lacroix Desmazes, Sebastien ^a  

^a INSERM   (France)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; B LYMPHOCYTE RECEPTOR; BLOOD CLOTTING FACTOR 7; BLOOD CLOTTING FACTOR 8; BLOOD CLOTTING FACTOR 9; CD4 ANTIGEN; CYTOKINE ANTIBODY; EPITOPE; ERYTHROPOIETIN; ETANERCEPT; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GROWTH HORMONE; IMMUNOSUPPRESSIVE AGENT; INSULIN; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 2; RECOMBINANT DNA; RECOMBINANT PROTEIN; SALCATONIN; STAPHYLOKINASE; STEROID; STREPTOKINASE; T LYMPHOCYTE RECEPTOR; VON WILLEBRAND FACTOR; PROTEIN;

ALLOIMMUNIZATION; ANAPHYLACTIC SHOCK; ANEMIA; ANTIGEN PRESENTING CELL; CELL INTERACTION; COMPUTER MODEL; CYSTIC FIBROSIS; DIABETES MELLITUS; ENDOCYTOSIS; GENE INTERACTION; HEALTH CARE COST; HEART INFARCTION; HEMOPHILIA; HEMOPHILIA A; HEMOPHILIA B; HEPATITIS C; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOGENICITY; INFLAMMATION; MICROENVIRONMENT; MULTIPLE SCLEROSIS; NEOPLASM; NEUTROPENIA; NONHUMAN; PAGET BONE DISEASE; PITUITARY DWARFISM; PREDICTIVE VALIDITY; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PROCESSING; SHORT SURVEY; SUBSTITUTION THERAPY; SYSTEMIC LUPUS ERYTHEMATOSUS; UNSPECIFIED SIDE EFFECT; VON WILLEBRAND DISEASE; ANIMAL; IMMUNOGENETICS; IMMUNOLOGY; METABOLISM; REVIEW;

ANIMALS; ANTIGEN-PRESENTING CELLS; ENDOCYTOSIS; HUMANS; IMMUNOGENETICS; INFLAMMATION; PROTEINS;

EID: 49649105287     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.3.1609     Document Type: Short Survey

References (102)

1. Pedotti, R., D. Mitchell, J. Wedemeyer, M. Karpuj, D. Chabas, E. M. Hattab, M. Tsai, S. J. Galli, and L. Steinman. 2001. An unexpected version of horror autotoxicus: anaphylactic shock to a self-peptide. Nat. Immunol. 2: 216-222.
2. Rosenberg, A. S. 2003. Immunogenicity of biological therapeutics: a hierarchy of concerns. Dev. Biol. 112: 15-21.
3. Rosenberg, A. S. 2006. Effects of protein aggregates: an immunologic perspective. AAPS J. 8: E501-507.
4. Schellekens, H. 2002. Immunogenicity of therapeutic proteins: clinical implications and future prospects. Clin. Ther. 24: 1720-1740.
5. Kadar, J. G., J. Schuster, and N. Hunzelmann. 2007. IgE-mediated anaphylactic reaction to purified and recombinant factor VIII in a patient with severe haemophilia A. Haemophilia 13: 104-105.
6. Shibata, M., M. Shima, H. Misu, Y. Okimoto, J. C. Giddings, and A. Yoshioka. 2003. Management of haemophilia B inhibitor patients with anaphylactic reactions to FIX concentrates. Haemophilia 9: 269-271.
7. Gringeri, A., L. G. Mantovani, L. Scalone, and P. M. Mannucci. 2003. Cost of care and quality of life for patients with hemophilia complicated by inhibitors: the COCIS Study Group. Blood 102: 2358-2363.
8. Barbosa, M. D., and E. Celis. 2007. Immunogenicity of protein therapeutics and the interplay between tolerance and antibody responses. Drug Discov. Today 12: 674-681.
9. Schellekens, H. 2002. Bioequivalence and the immunogenicity of biopharmaceuticals. Nat. Rev. Drug Discov. 1: 457-462.
10. De Groot, A. S., and D. W. Scott. 2007. Immunogenicity of protein therapeutics. Trends Immunol. 28: 482-490.
11. Delamarre, L., M. Pack, H. Chang, I. Mellman, and E. S. Trombetta. 2005. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307: 1630-1634.
12. Trombetta, E. S., and I. Mellman. 2005. Cell biology of antigen processing in vitro and in vivo. Annu. Rev. Immunol. 23: 975-1028.
13. Tacken, P. J., I. J. de Vries, R. Torensma, and C. G. Figdor. 2007. Dendritic-cell immunotherapy: from ex vivo loading to in vivo targeting. Nat. Rev. Immunol. 7: 790-802.
14. Dudziak, D., A. O. Kamphorst, G. F. Heidkamp, V. R. Buchholz, C. Trumpfheller, S. Yamazaki, C. Cheong, K. Liu, H. W. Lee, C. G. Park, et al. 2007. Differential antigen processing by dendritic cell subsets in vivo. Science 315: 107-111.
15. Shortman, K., and Y. J. Liu. 2002. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2: 151-161.
16. Leenen, P. J., K. Radosevic, J. S. Voerman, B. Salomon, N. van Rooijen, D. Klatzmann, and W. van Ewijk. 1998. Heterogeneity of mouse spleen dendritic cells: in vivo phagocytic activity, expression of macrophage markers, and subpopulation turnover. J. Immunol. 160: 2166-2173.
17. Langenkamp, A., M. Messi, A. Lanzavecchia, and F. Sallusto. 2000. Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat. Immunol. 1: 311-316.
18. d'Ostiani, C. F., G. Del Sero, A. Bacci, C. Montagnoli, A. Spreca, A. Mencacci, P. Ricciardi-Castagnoli, and L. Romani. 2000. Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans. Implications for initiation of T helper cell immunity in vitro and in vivo. J. Exp. Med. 191: 1661-1674.
19. Vandenabeele, S., H. Hochrein, N. Mavaddat, K. Winkel, and K. Shortman. 2001. Human thymus contains 2 distinct dendritic cell populations. Blood 97: 1733-1741.
20. +, and mature interdigitating dendritic cells. J. Clin. Invest. 107: 835-844.
21. Mebius, R. E., and G. Kraal. 2005. Structure and function of the spleen. Nat. Rev. Immunol. 5: 606-616.
22. Junt, T., E. A. Moseman, M. Iannacone, S. Massberg, P. A. Lang, M. Boes, K. Fink, S. E. Henrickson, D. M. Shayakhmetov, N. C. Di Paolo, et al. 2007. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 450: 110-114.
23. + macrophages. J. Clin. Invest. 117: 2517-2525.
24. Ciavarra, R. P., L. Taylor, A. R. Greene, N. Yousefieh, D. Horeth, N. van Rooijen, C. Steel, B. Gregory, M. Birkenbach, and M. Sekellick. 2005. Impact of macrophage and dendritic cell subset elimination on antiviral immunity, viral clearance and production of type 1 interferon. Virology 342: 177-189.
25. Sponaas, A. M., E. T. Cadman, C. Voisine, V. Harrison, A. Boonstra, A. O'Garra, and J. Langhorne. 2006. Malaria infection changes the ability of splenic dendritic cell populations to stimulate antigen-specific T cells. J. Exp. Med. 203: 1427-1433.
26. Shin, J. S., M. Ebersold, M. Pypaert, L. Delamarre, A. Hartley, and I. Mellman. 2006. Surface expression of MHC class II in dendritic cells is controlled by regulated ubiquitination. Nature 444: 115-118.
27. Guermonprez, P., J. Valladeau, L. Zitvogel, C. Thery, and S. Amigorena. 2002. Antigen presentation and T cell stimulation by dendritic cells. Annu. Rev. Immunol. 20: 621-667.
28. Devaraj, S., M. R. Dasu, J. Rockwood, W. Winter, S. C. Griffen, and I. Jialal. 2008. Increased toll-like receptor (TLR) 2 and TLR4 expression in monocytes from patients with type 1 diabetes: further evidence of a proinflammatory state. J. Clin. Endocrinol. Metab. 93: 578-583.
29. Hornell, T. M., G. W. Beresford, A. Bushey, J. M. Boss, and E. D. Mellins. 2003. Regulation of the class II MHC pathway in primary human monocytes by granulocyte-macrophage colony-stimulating factor. J. Immunol. 171: 2374-2383.
30. Rifkin, I. R., E. A. Leadbetter, L. Busconi, G. Viglianti, and A. Marshak-Rothstein. 2005. Toll-like receptors, endogenous ligands, and systemic autoimmune disease. Immunol. Rev. 204: 27-42.
31. Barrat, F. J., T. Meeker, J. Gregorio, J. H. Chan, S. Uematsu, S. Akira, B. Chang, O. Duramad, and R. L. Coffman. 2005. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med. 202: 1131-1139.
32. Shi, Y., J. E. Evans, and K. L. Rock. 2003. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425: 516-521.
33. Figueiredo, R. T., P. L. Fernandez, D. S. Mourao-Sa, B. N. Porto, F. F. Dutra, L. S. Alves, M. F. Oliveira, P. L. Oliveira, A. V. Graca-Souza, and M. T. Bozza. 2007. Characterization of heme as activator of Toll-like receptor 4. J. Biol. Chem. 282: 20221-20229.
34. +FoxP3+ regulatory T cells in autoimmune diseases. Nat. Clin. Pract. Rheumatol. 3: 619-626.
35. Obst, R., H. M. van Santen, R. Melamed, A. O. Kamphorst, C. Benoist, and D. Mathis. 2007. Sustained antigen presentation can promote an immunogenic T cell response, like dendritic cell activation. Proc. Natl. Acad. Sci. USA 104: 15460-15465.
36. Carayanniotis, G., and B. H. Barber. 1987. Adjuvant-free IgG responses induced with antigen coupled to antibodies against class II MHC. Nature 327: 59-61.
37. De Groot, A. S., and L. Moise. 2007. Prediction of immunogenicity for therapeutic proteins: state of the art. Curr. Opin. Drug. Discov. Devel. 10: 332-340.
38. Lazarski, C. A., F. A. Chaves, S. A. Jenks, S. Wu, K. A. Richards, J. M. Weaver, and A. J. Sant. 2005. The kinetic stability of MHC class II:peptide complexes is a key parameter that dictates immunodominance. Immunity 23: 29-40.
39. Barbosa, M. D., J. Vielmetter, S. Chu, D. D. Smith, and J. Jacinto. 2006. Clinical link between MHC class II haplotype and interferon-β (IFN-β) immunogenicity. Clin. Immunol. 118: 42-50.
40. Hay, C. R., W. Ollier, L. Pepper, A. Cumming, S. Keeney, A. C. Goodeve, B. T. Colvin, F. G. Hill, F. E. Preston, and I. R. Peake. 1997. HLA class II profile: a weak determinant of factor VIII inhibitor development in severe haemophilia A. UKHCDO Inhibitor Working Party. Thromb. Haemostasis 77: 234-237.
41. Oldenburg, J., J. K. Picard, R. Schwaab, H. H. Brackmann, E. G. Tuddenham, and E. Simpson. 1997. HLA genotype of patients with severe haemophilia A due to intron 22 inversion with and without inhibitors of factor VIII. Thromb. Haemostasis 77: 238-242.
42. Koren, E., A. S. De Groot, V. Jawa, K. D. Beck, T. Boone, D. Rivera, L. Li, D. Mytych, M. Koscec, D. Weeraratne, et al. 2007. Clinical validation of the "in silico" prediction of immunogenicity of a human recombinant therapeutic protein. Clin. Immunol. 124: 26-32.
43. Marshall, S. A., G. A. Lazar, A. J. Chirino, and J. R. Desjarlais. 2003. Rational design and engineering of therapeutic proteins. Drug Discov. Today 8: 212-221.
44. Jaber, A., and M. Baker. 2007. Assessment of the immunogenicity of different interferon β-1a formulations using ex vivo T-cell assays. J. Pharm. Biomed. Anal. 43: 1256-1261.
45. Hobeika, A. C., M. A. Morse, T. Osada, M. Ghanayem, D. Niedzwiecki, R. Barrier, H. K. Lyerly, and T. M. Clay. 2005. Enumerating antigen-specific T-cell responses in peripheral blood: a comparison of peptideMHCTetramer, ELISpot, and intracellular cytokine analysis. J. Immunother. 28: 63-72.
46. Steere, A. C., W. Klitz, E. E. Drouin, B. A. Falk, W. W. Kwok, G. T. Nepom, and L. A. Baxter-Lowe. 2006. Antibiotic-refractory Lyme arthritis is associated with HLA-DR molecules that bind a Borrelia burgdorferi peptide. J. Exp. Med. 203: 961-971.
47. McMurry, J. A., S. H. Gregory, L. Moise, D. Rivera, S. Buus, and A. S. De Groot. 2007. Diversity of Francisella tularensis Schu4 antigens recognized by T lymphocytes after natural infections in humans: identification of candidate epitopes for inclusion in a rationally designed tularemia vaccine. Vaccine 25: 3179-3191.
48. Feldmann, M., F. M. Brennan, R. O. Williams, A. P. Cope, D. L. Gibbons, P. D. Katsikis, and R. N. Maini. 1992. Evaluation of the role of cytokines in autoimmune disease: the importance of TNF α in rheumatoid arthritis. Prog. Growth Factor Res. 4: 247-255.
49. Sachs, D. H. 2003. Tolerance: of mice and men. J. Clin. Invest. 111: 1819-1821.
50. Mestas, J., and C. C. Hughes. 2004. Of mice and not men: differences between mouse and human immunology. J. Immunol. 172: 2731-2738.
51. t Hart, B. A., S. Amor, and M. Jonker. 2004. Evaluating the validity of animal models for research into therapies for immune-based disorders. Drug Discov. Today 9: 517-524.
52. Dixit, R., and U. A. Boelsterli. 2007. Healthy animals and animal models of human disease(s) in safety assessment of human pharmaceuticals, including therapeutic antibodies. Drug Discov. Today 12: 336-342.
53. Kong, Y. C., L. C. Lomo, R. W. Motte, A. A. Giraldo, J. Baisch, G. Strauss, G. J. Hammerling, and C. S. David. 1996. HLA-DRB1 polymorphism determines susceptibility to autoimmune thyroiditis in transgenic mice: definitive association with HLA-DRB1*0301 (DR3) gene. J. Exp. Med. 184: 1167-1172.
54. Pan, S., T. Trejo, J. Hansen, M. Smart, and C. S. David. 1998. HLA-DR4 (DRB1*0401) transgenic mice expressing an altered CD4-binding site: specificity and magnitude of DR4-restricted T cell response. J. Immunol. 161: 2925-2929.
55. Shirai, M., T. Arichi, M. Nishioka, T. Nomura, K. Ikeda, K. Kawanishi, V. H. Engelhard, S. M. Feinstone, and J. A. Berzofsky. 1995. CTL responses of HLA-A2.1-transgenic mice specific for hepatitis C viral peptides predict epitopes for CTL of humans carrying HLA-A2.1. J. Immunol. 154: 2733-2742.
56. Man, S., M. H. Newberg, V. L. Crotzer, C. J. Luckey, N. S. Williams, Y. Chen, E. L. Huczko, J. P. Ridge, and V. H. Engelhard. 1995. Definition of a human T cell epitope from influenza A non-structural protein 1 using HLA-A2.1 transgenic mice. Int. Immunol. 7: 597-605.
57. Charo, J., M. Sundback, A. Geluk, T. Ottenhoff, and R. Kiessling. 2001. DNA immunization of HLA transgenic mice with a plasmid expressing mycobacterial heat shock protein 65 results in HLA class I- and II-restricted T cell responses that can be augmented by cytokines. Hum. Gene Ther. 12: 1797-1804.
58. Ishioka, G. Y., J. Fikes, G. Hermanson, B. Livingston, C. Crimi, M. Qin, M. F. del Guercio, C. Oseroff, C. Dahlberg, J. Alexander, et al. 1999. Utilization of MHC class I transgenic mice for development of minigene DNA vaccines encoding multiple HLA-restricted CTL epitopes. J. Immunol. 162: 3915-3925.
59. Ottesen, J. L., P. Nilsson, J. Jami, D. Weilguny, M. Duhrkop, D. Bucchini, S. Havelund, and J. M. Fogh. 1994. The potential immunogenicity of human insulin and insulin analogues evaluated in a transgenic mouse model. Diabetologia 37: 1178-1185.
60. Palleroni, A. V., A. Aglione, M. Labow, M. J. Brunda, S. Pestka, F. Sinigaglia, G. Garotta, J. Alsenz, and A. Braun. 1997. Interferon immunogenicity: preclinical evaluation of interferon-α 2a. J. Interferon Cytokine Res. 17(Suppl. 1): S23-S27.
61. Stewart, T. A., P. G. Hollingshead, S. L. Pitts, R. Chang, L. E. Martin, and H. Oakley. 1989. Transgenic mice as a model to test the immunogenicity of proteins altered by site-specific mutagenesis. Mol. Biol. Med. 6: 275-281.
62. Healey, J. F., E. T. Parker, R. T. Barrow, T. J. Langley, W. R. Church, and P. Lollar. 2007. The humoral response to human factor VIII in hemophilia A mice. J. Thromb. Haemost. 5: 512-519.
63. Delignat, S., S. Dasgupta, S. Andre, A. M. Navarrete, S. V. Kaveri, J. Bayry, M. H. Andre, S. Chtourou, Z. Tellier, and S. Lacroix-Desmazes. 2007. Comparison of the immunogenicity of different therapeutic preparations of human factor VIII in the murine model of hemophilia A. Haematologica 92: 1423-1426.
64. Perini, P., A. Facchinetti, P. Bulian, A. R. Massaro, D. D. Pascalis, A. Bertolotto, G. Biasi, and P. Gallo. 2001. Interferon-β(INF-β) antibodies in interferon-β1a- and interferon-β1b-treated multiple sclerosis patients. Prevalence, kinetics, cross-reactivity, and factors enhancing interferon-β immunogenicity in vivo. Eur. Cytokine Network 12: 56-61.
65. Ross, C., K. M. Clemmesen, M. Svenson, P. S. Sorensen, N. Koch-Henriksen, G. L. Skovgaard, and K. Bendtzen. 2000. Immunogenicity of interferon-β in multiple sclerosis patients: influence of preparation, dosage, dose frequency, and route of administration. Danish Multiple Sclerosis Study Group. Ann. Neurol. 48: 706-712.
66. Levy, F., R. Muff, S. Dotti-Sigrist, M. A. Dambacher, and J. A. Fischer. 1988. Formation of neutralizing antibodies during intranasal synthetic salmon calcitonin treatment of Paget's disease. J. Clin. Endocrinol. Metab. 67: 541-545.
67. Eisenberg, J. D., M. L. Aitken, H. L. Dorkin, I. R. Harwood, B. W. Ramsey, D. V. Schidlow, R. W. Wilmott, M. E. Wohl, H. J. Fuchs, D. H. Christiansen, and A. L. Smith. 1997. Safety of repeated intermittent courses of aerosolized recombinant human deoxyribonuclease in patients with cystic fibrosis. J. Pediatr. 131: 118-124.
68. Morishita, M., and N. A. Peppas. 2006. Is the oral route possible for peptide and protein drug delivery? Drug Discov. Today 11: 905-910.
69. Johansson, A., A. Erlandsson, D. Eriksson, A. Ullen, P. Holm, B. E. Sundstrom, K. H. Roux, and T. Stigbrand. 2002. Idiotypic-anti-idiotypic complexes and their in vivo metabolism. Cancer 94: 1306-1313.
70. Wagner, C. L., A. Schantz, E. Barnathan, A. Olson, M. A. Mascelli, J. Ford, L. Damaraju, T. Schaible, R. N. Maini, and J. E. Tcheng. 2003. Consequences of immunogenicity to the therapeutic monoclonal antibodies ReoPro and Remicade. Dev. Biol. 112: 37-53.
71. Tabrizi, M. A., C. M. Tseng, and L. K. Roskos. 2006. Elimination mechanisms of therapeutic monoclonal antibodies. Drug Discov. Today 11: 81-88.
72. Chirino, A. J., M. L. Ary, and S. A. Marshall. 2004. Minimizing the immunogenicity of protein therapeutics. Drug Discov. Today 9: 82-90.
73. Harris, J. M., N. E. Martin, and M. Modi. 2001. Pegylation: a novel process for modifying pharmacokinetics. Clin. Pharmacokinet. 40: 539-551.
74. Savoca, K. V., A. Abuchowski, T. van Es, F. F. Davis, and N. C. Palczuk. 1979. Preparation of a non-immunogenic arginase by the covalent attachment of polyethylene glycol. Biochim. Biophys. Acta 578: 47-53.
75. Hershfield, M. S., S. Chaffee, L. Koro-Johnson, A. Mary, A. A. Smith, and S. A. Short. 1991. Use of site-directed mutagenesis to enhance the epitope-shielding effect of covalent modification of proteins with polyethylene glycol. Proc. Natl. Acad. Sci. USA 88: 7185-7189.
76. Bailon, P., A. Palleroni, C. A. Schaffer, C. L. Spence, W. J. Fung, J. E. Porter, G. K. Ehrlich, W. Pan, Z. X. Xu, M. W. Modi, et al. 2001. Rational design of a potent, long-lasting form of interferon: a 40 kDa branched polyethylene glycol-conjugated interferon α-2a for the treatment of hepatitis C. Bioconjug. Chem. 12: 195-202.
77. Komba, S., O. Werdelin, T. Jensen, and M. Meldal. 2000. Synthesis of tumor associated sialyl-T-glycopeptides and their immunogenicity. J. Pept. Sci. 6: 585-593.
78. Tangri, S., B. R. Mothe, J. Eisenbraun, J. Sidney, S. Southwood, K. Briggs, J. Zinckgraf, P. Bilsel, M. Newman, R. Chesnut, et al. 2005. Rationally engineered therapeutic proteins with reduced immunogenicity. J. Immunol. 174: 3187-3196.
79. Lindstedt, M., B. Johansson-Lindbom, and C. A. Borrebaeck. 2002. Global reprogramming of dendritic cells in response to a concerted action of inflammatory mediators. Int. Immunol. 14: 1203-1213.
80. Deslee, G., A. S. Charbonnier, H. Hammad, G. Angyalosi, I. Tillie-Leblond, A. Mantovani, A. B. Tonnel, and J. Pestel. 2002. Involvement of the mannose receptor in the uptake of Der p 1, a major mite allergen, by human dendritic cells. J. Allergy Clin. Immunol. 110: 763-770.
81. Wollenberg, A., M. Mommaas, T. Oppel, E. M. Schottdorf, S. Gunther, and M. Moderer. 2002. Expression and function of the mannose receptor CD206 on epidermal dendritic cells in inflammatory skin diseases. J. Invest. Dermatol. 118: 327-334.
82. + regulatory T-cell functions in rheumatoid arthritis by cytokine-targeted monoclonal antibody therapy. Drug Discov. Today 12: 548-552.
83. + T lymphocytes. Proc. Natl. Acad. Sci. USA 104: 8965-8970.
84. Dasgupta, S., Y. Repesse, J. Bayry, A. M. Navarrete, B. Wootla, S. Delignat, T. Irinopoulou, C. Kamate, J. M. Saint-Remy, M. Jacquemin, et al. 2007. VWF protects FVIII from endocytosis by dendritic cells and subsequent presentation to immune effectors. Blood 109: 610-612.
85. Fineberg, S. E., T. T. Kawabata, D. Finco-Kent, R. J. Fountaine, G. L. Finch, and A. S. Krasner. 2007. Immunological responses to exogenous insulin. Endocr. Rev. 28: 625-652.
86. Romer, T., F. Peter, P. Saenger, J. Starzyk, B. Koehler, E. Korman, M. Walczak, R. Wasik, M. Ginalska-Malinowska, E. Solyom, and A. Berghout. 2007. Efficacy and safety of a new ready-to-use recombinant human growth hormone solution. J. Endocrinol. Invest. 30: 578-589.
87. DiMichele, D. 2007. Inhibitor development in haemophilia B: an orphan disease in need of attention. Br. J. Haematol. 138: 305-315.
88. Gouw, S. C., H. M. van den Berg, S. le Cessie, and J. G. van der Bom. 2007. Treatment characteristics and the risk of inhibitor development: a multicenter cohort study among previously untreated patients with severe hemophilia A. J. Thromb. Haemost. 5: 1383-1390.
89. Bergamaschini, L., P. M. Mannucci, A. B. Federici, R. Coppola, S. Guzzoni, and A. Agostoni. 1995. Posttransfusion anaphylactic reactions in a patient with severe von Willebrand disease: role of complement and alloantibodies to von Willebrand factor. J. Lab. Clin. Med. 125: 348-355.
90. Casadevall, N. 2003. Pure red cell aplasia and anti-erythropoietin antibodies in patients treated with epoetin. Nephrol. Dial. Transplant. 18 Suppl 8: viii37- 41.
91. Rosenschein, U., R. Lenz, J. Radnay, T. Ben Tovim, and L. A. Rozenszajn. 1991. Streptokinase immunogenicity in thrombolytic therapy for acute myocardial infarction. Isr. J. Med. Sci. 27: 541-545.
92. Vanderschueren, S. M., J. M. Stassen, and D. Collen. 1994. On the immunogenicity of recombinant staphylokinase in patients and in animal models. Thromb. Haemost. 72: 297-301.
93. Lawley, W. J., S. Fletcher, I. B. Squire, K. L. Woods, and C. R. Hewitt. 2000. T-cell recognition of discrete regions of the thrombolytic drug streptokinase. Clin. Sci. (Lond.) 99: 239-246.
94. Porter, S. 2001. Human immune response to recombinant human proteins. J. Pharm. Sci. 90: 1-11.
95. Antonelli, G., G. Giannelli, M. Currenti, E. Simeoni, S. Del Vecchio, F. Maggi, M. Pistello, L. Roffi, G. Pastore, L. Chemello, and F. Dianzani. 1996. Antibodies to interferon (IFN) in hepatitis C patients relapsing while continuing recombinant IFN-α2 therapy. Clin. Exp. Immunol. 104: 384-387.
96. Prummer, O. 1997. Treatment-induced antibodies to interleukin-2. Biotherapy 10: 15-24.
97. Ragnhammar, P., H. J. Friesen, J. E. Frodin, A. K. Lefvert, M. Hassan, A. Osterborg, and H. Mellstedt. 1994. Induction of anti-recombinant human granulocyte-macrophage colony-stimulating factor (Escherichia coli-derived) antibodies and clinical effects in nonimmunocompromised patients. Blood 84: 4078-4087.
98. Laricchia-Robbio, L., S. Moscato, A. Genua, A. M. Liberati, and R. P. Revoltella. 1997. Naturally occurring and therapy-induced antibodies to human granulocyte colony-stimulating factor (G-CSF) in human serum. J. Cell. Physiol. 173: 219-226.
99. Husson, R. N., Y. Chung, J. Mordenti, K. M. Butler, S. Chen, A. M. Duliege, P. Brouwers, P. Jarosinski, B. U. Mueller, A. Ammann, et al. 1992. Phase I study of continuous-infusion soluble CD4 as a single agent and in combination with oral dideoxyinosine therapy in children with symptomatic human immunodeficiency virus infection. J. Pediatr. 121: 627-633.
100. Lenercept Multiple Sclerosis Study Group and University of British Columbia MS/MRI Analysis Group 1999. TNF neutralization in MS: results of a randomized, placebo-controlled multicenter study. Neurology 53: 457-465.
101. Llorente, L., Y. Richaud-Patin, C. Garcia-Padilla, E. Claret, J. Jakez-Ocampo, M. H. Cardiel, J. Alcocer-Varela, L. Grangeot-Keros, D. Alarcon-Segovia, J. Wijdenes, et al. 2000. Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum. 43: 1790-1800.
102. Bayry, J., S. Lacroix-Desmazes, M. D. Kazatchkine, and S. V. Kaveri. 2007. Monoclonal antibody and intravenous immunoglobulin therapy for rheumatic diseases: rationale and mechanisms of action. Nat. Clin. Pract. Rheumatol. 3: 262-272.